Section: Evolutionary Biology
Topic: Evolution, Biology of interactions, Population biology

Parasitic success and venom composition evolve upon specialization of parasitoid wasps to different host species

10.24072/pcjournal.28 - Peer Community Journal, Volume 1 (2021), article no. e51.

Get full text PDF Peer reviewed and recommended by PCI
article image

Female endoparasitoid wasps usually inject venom into hosts to suppress their immune response and ensure offspring development. However, the parasitoids ability to evolve towards increased success on a given host simultaneously with the evolution of the composition of its venom has never been demonstrated. Here, we designed an experimental evolution to address this question. We crossed two parasitoid lines of Leptopilina boulardi differing both in parasitic success on different Drosophila hosts and venom composition. F2 descendants were reared on three different Drosophila species for nine generations. We tested for evolution of parasitic success over the generations and for the capacity of parasitoids selected on a given host to succeed on another host. We also tested whether the venom composition - based on a statistical analysis of the variation in intensity of the venom protein bands on SDS-PAGE 1D - evolved in response to different host species. Results showed a specialization of the parasitoids on their selection host and a rapid and differential evolution of the venom composition according to the host. Overall, data suggest a high potential for parasitoids to adapt to a new host, which may have important consequences in the field as well in the context of biological control.

Published online:
DOI: 10.24072/pcjournal.28
Type: Research article

Cavigliasso, Fanny 1, 2; Mathé-Hubert, Hugo 1, 2; Gatti, Jean-Luc 2; Colinet, Dominique 2; Poirié, Marylène 2

1 Present address: Department of Ecology and Evolution, University of Lausanne – Lausanne, Switzerland
2 Université Côte d’Azur, INRA, CNRS, ISA – Sophia Antipolis, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Cavigliasso, Fanny and Math\'e-Hubert, Hugo and Gatti, Jean-Luc and Colinet, Dominique and Poiri\'e, Maryl\`ene},
     title = {Parasitic success and venom composition evolve upon specialization of parasitoid wasps to different host species},
     journal = {Peer Community Journal},
     eid = {e51},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.28},
     url = {}
AU  - Cavigliasso, Fanny
AU  - Mathé-Hubert, Hugo
AU  - Gatti, Jean-Luc
AU  - Colinet, Dominique
AU  - Poirié, Marylène
TI  - Parasitic success and venom composition evolve upon specialization of parasitoid wasps to different host species
JO  - Peer Community Journal
PY  - 2021
VL  - 1
PB  - Peer Community In
UR  -
DO  - 10.24072/pcjournal.28
ID  - 10_24072_pcjournal_28
ER  - 
%0 Journal Article
%A Cavigliasso, Fanny
%A Mathé-Hubert, Hugo
%A Gatti, Jean-Luc
%A Colinet, Dominique
%A Poirié, Marylène
%T Parasitic success and venom composition evolve upon specialization of parasitoid wasps to different host species
%J Peer Community Journal
%D 2021
%V 1
%I Peer Community In
%R 10.24072/pcjournal.28
%F 10_24072_pcjournal_28
Cavigliasso, Fanny; Mathé-Hubert, Hugo; Gatti, Jean-Luc; Colinet, Dominique; Poirié, Marylène. Parasitic success and venom composition evolve upon specialization of parasitoid wasps to different host species. Peer Community Journal, Volume 1 (2021), article  no. e51. doi : 10.24072/pcjournal.28.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100124

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Anderson, M. J. Permutational Multivariate Analysis of Variance ( PERMANOVA ), Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef: Statistics Reference Online, (2017), pp. 1-15 | DOI

[2] Asgari, S.; Rivers, D. B. Venom Proteins from Endoparasitoid Wasps and Their Role in Host-Parasite Interactions, Annual Review of Entomology, Volume 56 (2011) no. 1, pp. 313-335 | DOI

[3] Barlow, A.; Pook, C. E.; Harrison, R. A.; Wüster, W. Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution, Proceedings of the Royal Society B: Biological Sciences, Volume 276 (2009) no. 1666, pp. 2443-2449 | DOI

[4] Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Usinglme4, Journal of Statistical Software, Volume 67 (2015) no. 1, pp. 1-48 | DOI

[5] Bolker, B. M.; Brooks, M. E.; Clark, C. J.; Geange, S. W.; Poulsen, J. R.; Stevens, M. H. H.; White, J.-S. S. Generalized linear mixed models: a practical guide for ecology and evolution, Trends in Ecology & Evolution, Volume 24 (2009) no. 3, pp. 127-135 | DOI

[6] Carton, Y.; Bouletreau, M.; van Alphen, J.; van Lenteren, J. The Drosophila parasitic wasps In: The genetics and biology of Drosophila (1986), pp. 347-394

[7] Cavigliasso; Mathé-Hubert; Kremmer; Rebuf; Gatti; Malausa; Colinet; Poirié Rapid and Differential Evolution of the Venom Composition of a Parasitoid Wasp Depending on the Host Strain, Toxins, Volume 11 (2019) no. 11 | DOI

[8] Cerenius, L.; Lee, B. L.; Söderhäll, K. The proPO-system: pros and cons for its role in invertebrate immunity, Trends in Immunology, Volume 29 (2008) no. 6, pp. 263-271 | DOI

[9] Chung, Y.; Rabe-Hesketh, S.; Dorie, V.; Gelman, A.; Liu, J. A Nondegenerate Penalized Likelihood Estimator for Variance Parameters in Multilevel Models, Psychometrika, Volume 78 (2013) no. 4, pp. 685-709 | DOI

[10] Colinet, D.; Deleury, E.; Anselme, C.; Cazes, D.; Poulain, J.; Azema-Dossat, C.; Belghazi, M.; Gatti, J.-L.; Poirié, M. Extensive inter- and intraspecific venom variation in closely related parasites targeting the same host: The case of Leptopilina parasitoids of Drosophila, Insect Biochemistry and Molecular Biology, Volume 43 (2013) no. 7, pp. 601-611 | DOI

[11] Colinet, D.; Dubuffet, A.; Cazes, D.; Moreau, S.; Drezen, J.-M.; Poirié, M. A serpin from the parasitoid wasp Leptopilina boulardi targets the Drosophila phenoloxidase cascade, Developmental & Comparative Immunology, Volume 33 (2009) no. 5, pp. 681-689 | DOI

[12] Colinet, D.; Kremmer, L.; Lemauf, S.; Rebuf, C.; Gatti, J.-L.; Poirié, M. Development of RNAi in a Drosophila endoparasitoid wasp and demonstration of its efficiency in impairing venom protein production, Journal of Insect Physiology, Volume 63 (2014), pp. 56-61 | DOI

[13] Colinet, D.; Mathé-Hubert, H.; Allemand, R.; Gatti, J.-L.; Poirié, M. Variability of venom components in immune suppressive parasitoid wasps: From a phylogenetic to a population approach, Journal of Insect Physiology, Volume 59 (2013) no. 2, pp. 205-212 | DOI

[14] Colinet, D.; Schmitz, A.; Cazes, D.; Gatti, J.-L.; Poirié, M. The Origin of Intraspecific Variation of Virulence in an Eukaryotic Immune Suppressive Parasite, PLoS Pathogens, Volume 6 (2010) no. 11 | DOI

[15] Colinet, D.; Schmitz, A.; Depoix, D.; Crochard, D.; Poirié, M. Convergent Use of RhoGAP Toxins by Eukaryotic Parasites and Bacterial Pathogens, PLoS Pathogens, Volume 3 (2007) no. 12 | DOI

[16] Dennis, A. B.; Patel, V.; Oliver, K. M.; Vorburger, C. Parasitoid gene expression changes after adaptation to symbiont-protected hosts, Evolution, Volume 71 (2017) no. 11, pp. 2599-2617 | DOI

[17] Dion, E.; Zélé, F.; Simon, J.-C.; Outreman, Y. Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts, Journal of Evolutionary Biology, Volume 24 (2011) no. 4, pp. 741-750 | DOI

[18] Dixon, P. VEGAN, a package of R functions for community ecology, Journal of Vegetation Science, Volume 14 (2003) no. 6, pp. 927-930 | DOI

[19] Dray, S.; Dufour, A.-B. Theade4Package: Implementing the Duality Diagram for Ecologists, Journal of Statistical Software, Volume 22 (2007) no. 4, pp. 1-20 | DOI

[20] Dubuffet, A.; Alvarez, C. I. R.; Drezen, J.-M.; van Alphen, J. J. M.; Poirie, M. Do parasitoid preferences for different host species match virulence?, Physiological Entomology, Volume 31 (2006) no. 2, pp. 170-177 | DOI

[21] Dubuffet, A.; Colinet, D.; Anselme, C.; Dupas, S.; Carton, Y.; Poirié, M. Chapter 6 Variation of Leptopilina boulardi Success in Drosophila Hosts, Advances in Parasitology Volume 70, Elsevier, 2009, pp. 147-188 | DOI

[22] Dubuffet, A.; Dupas, S.; Frey, F.; Drezen, J.-M.; Poirié, M.; Carton, Y. Genetic interactions between the parasitoid wasp Leptopilina boulardi and its Drosophila hosts, Heredity, Volume 98 (2006) no. 1, pp. 21-27 | DOI

[23] Dudzic, J. P.; Kondo, S.; Ueda, R.; Bergman, C. M.; Lemaitre, B. Drosophila innate immunity: regional and functional specialization of prophenoloxidases, BMC Biology, Volume 13 (2015) no. 1 | DOI

[24] Dupas, S.; Boscaro, M. Geographic variation and evolution of immunosuppressive genes in a Drosophila parasitoid, Ecography, Volume 22 (1999) no. 3, pp. 284-291 | DOI

[25] Dupas, S.; Dubuffet, A.; Carton, Y.; Poirié, M. Chapter 11 Local, Geographic and Phylogenetic Scales of Coevolution in Drosophila–Parasitoid Interactions, Advances in Parasitology Volume 70, Elsevier, 2009, pp. 281-295 | DOI

[26] Dupas, S. A single parasitoid segregating factor controls immune suppression in Drosophila, Journal of Heredity, Volume 89 (1998) no. 4, pp. 306-311 | DOI

[27] Evans, E. R. J.; Northfield, T. D.; Daly, N. L.; Wilson, D. T. Venom Costs and Optimization in Scorpions, Frontiers in Ecology and Evolution, Volume 7 (2019) | DOI

[28] Fellowes, M. D. E.; Kraaijeveld, A. R.; Godfray, H. C. J. Trade–off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 265 (1998) no. 1405, pp. 1553-1558 | DOI

[29] Fors, L.; Markus, R.; Theopold, U.; Ericson, L.; Hambäck, P. A. Geographic variation and trade-offs in parasitoid virulence, Journal of Animal Ecology, Volume 85 (2016) no. 6, pp. 1595-1604 | DOI

[30] Godfray, H. C. J. Parasitoids: behavioral and evolutionary ecology, Princeton University Press, 1994

[31] Harrison, X. A. A comparison of observation-level random effect and Beta-Binomial models for modelling overdispersion in Binomial data in ecology & evolution, PeerJ, Volume 3 (2015) | DOI

[32] Hita, M.; Espagne, E.; Lemeunier, F.; Pascual, L.; Carton, Y.; Periquet, G.; Poirié, M. Mapping candidate genes for Drosophila melanogaster resistance to the parasitoid wasp Leptopilina boulardi, Genetical Research, Volume 88 (2006) no. 2, pp. 81-91 | DOI

[33] Hothorn, T.; Bretz, F.; Westfall, P. Simultaneous Inference in General Parametric Models, Biometrical Journal, Volume 50 (2008) no. 3, pp. 346-363 | DOI

[34] Kim-Jo, C.; Gatti, J.-L.; Poirié, M. Drosophila Cellular Immunity Against Parasitoid Wasps: A Complex and Time-Dependent Process, Frontiers in Physiology, Volume 10 (2019) | DOI

[35] Kraaijeveld, A. R.; Hutcheson, K. A.; Limentani, E. C.; Godfray, H. C. J. Costs of counterdefenses to host resistance in a parasitoid of Drosophila, Evolution, Volume 55 (2001) no. 9, pp. 1815-1821 | DOI

[36] Labrosse, C.; Eslin, P.; Doury, G.; Drezen, J.; Poirié, M. Haemocyte changes in D. Melanogaster in response to long gland components of the parasitoid wasp Leptopilina boulardi: a Rho-GAP protein as an important factor, Journal of Insect Physiology, Volume 51 (2005) no. 2, pp. 161-170 | DOI

[37] Labrosse, C.; Stasiak, K.; Lesobre, J.; Grangeia, A.; Huguet, E.; Drezen, J.; Poirie, M. A RhoGAP protein as a main immune suppressive factor in the Leptopilina boulardi (Hymenoptera, Figitidae)–Drosophila melanogaster interaction, Insect Biochemistry and Molecular Biology, Volume 35 (2005) no. 2, pp. 93-103 | DOI

[38] Lapchin, L. Host‐Parasitoid Association and Diffuse Coevolution: When to Be a Generalist?, The American Naturalist, Volume 160 (2002) no. 2, pp. 245-254 | DOI

[39] Lenski, R. E. Experimental evolution and the dynamics of adaptation and genome evolution in microbial populations, The ISME Journal, Volume 11 (2017) no. 10, pp. 2181-2194 | DOI

[40] Luo, D.; Ding, C.; Huang, H. Linear discriminant analysis: new formulations and overfit analysis. Proceedings of the Twenty-Fifth AAAI Conference on Artificial Intelligence, AAAI 2011, San Francisco, California, USA, August 7-11, 2011, (2011)

[41] Mathé-Hubert, H.; Gatti, J.-L.; Colinet, D.; Poirié, M.; Malausa, T. Statistical analysis of the individual variability of 1D protein profiles as a tool in ecology: an application to parasitoid venom, Molecular Ecology Resources, Volume 15 (2015) no. 5, pp. 1120-1132 | DOI

[42] Mathé-Hubert, H.; Kremmer, L.; Colinet, D.; Gatti, J.-L.; Van Baaren, J.; Delava, É.; Poirié, M. Variation in the Venom of Parasitic Wasps, Drift, or Selection? Insights From a Multivariate QST Analysis, Frontiers in Ecology and Evolution, Volume 7 (2019) | DOI

[43] Moreau, S.; Asgari, S. Venom Proteins from Parasitoid Wasps and Their Biological Functions, Toxins, Volume 7 (2015) no. 7, pp. 2385-2412 | DOI

[44] Mrinalini; Siebert, A. L.; Wright, J.; Martinson, E.; Wheeler, D.; Werren, J. H. Parasitoid venom induces metabolic cascades in fly hosts, Metabolomics, Volume 11 (2014) no. 2, pp. 350-366 | DOI

[45] Nappi, A. J. Cellular immunity and pathogen strategies in combative interactions involving Drosophila hosts and their endoparasitic wasps, Invertebrate Survival Journal, Volume 7 (2010) no. 2, pp. 198-210

[46] Nappi, A.; Christensen, B. Melanogenesis and associated cytotoxic reactions: Applications to insect innate immunity, Insect Biochemistry and Molecular Biology, Volume 35 (2005) no. 5, pp. 443-459 | DOI

[47] Pinheiro, J.; Bates, D.; DebRoy, S.; Sarkar, D. R Core Team. 2018. nlme: linear and nonlinear mixed effects models. R package version 3.1-137, (2018)

[48] Poirié, M.; Colinet, D.; Gatti, J.-L. Insights into function and evolution of parasitoid wasp venoms, Current Opinion in Insect Science, Volume 6 (2014), pp. 52-60 | DOI

[49] Poirie, M.; Frey, F.; Hita, M.; Huguet, E.; Lemeunier, F.; Periquet, G.; Carton, Y. Drosophila resistance genes to parasitoids: chromosomal location and linkage analysis, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 267 (2000) no. 1451, pp. 1417-1421 | DOI

[50] Qiao, Z.; Zhou, L.; Huang, J. Z. Effective linear discriminant analysis for high dimensional, low sample size data. Proceedings of the World Congress on Engineering 2008 Vol II WCE 2008, July 2 - 4, 2008, London, U.K., (2008)

[51] Rouchet, R.; Vorburger, C. Experimental evolution of parasitoid infectivity on symbiont-protected hosts leads to the emergence of genotype specificity, Evolution, Volume 68 (2014) no. 6, pp. 1607-1616 | DOI

[52] Vlisidou, I.; Wood, W. Drosophila blood cells and their role in immune responses, FEBS Journal, Volume 282 (2015) no. 8, pp. 1368-1382 | DOI

[53] Wan, B.; Goguet, E.; Ravallec, M.; Pierre, O.; Lemauf, S.; Volkoff, A.-N.; Gatti, J.-L.; Poirié, M. Venom Atypical Extracellular Vesicles as Interspecies Vehicles of Virulence Factors Involved in Host Specificity: The Case of a Drosophila Parasitoid Wasp, Frontiers in Immunology, Volume 10 ((2019)) | DOI

Cited by Sources: